Abstract
Downward fluxes of biogenic silica and organic matter in the global ocean derive dominantly from the productivity of diatoms — phytoplankton with cell walls containing silica encased in an organic matrix1,2. As diatoms have an absolute requirement for silicon (as silicic acid)3, its supply into the photic zone — largely by silica dissolution and upwelling — controls diatom production (and consequently the biological uptake of atmospheric CO2 by the ocean) over vast oceanic areas4. Current biogeochemical models assume silica dissolution to be controlled by temperature, zooplankton grazing and diatom aggregation4,5, but the role of bacteria has not been established. Yet bacteria utilize about half of the organic matter derived from oceanic primary production6 by varied strategies, including attack on dead and living diatoms by using hydrolytic enzymes7,8, and could adventitiously hasten silica dissolution by degrading the organic matrix which protects diatom frustules from dissolution9,10. Here we report the results of experiments in which natural assemblages of marine bacteria dramatically increased silica dissolution from two species of lysed marine diatoms compared to bacteria-free controls. Silica dissolution accompanied, and was caused by, bacterial colonization and hydrolytic attack. Bacteria-mediated silicon regeneration rates varied with diatom type and bacterial assemblage; observed rates could explain most of the reported upper-ocean silicon regeneration5,11. Bacteria-mediated silicon regeneration may thus critically control diatom productivity and the cycling and fate of silicon and carbon in the ocean.
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References
Nelson, D. M., DeMaster, D. J., Dunbar, R. B. & Smith, W. O. J Cycling of organic carbon and biogenic silica in the Southern Ocean: estimates of water-column and sedimentary fluxes on the Ross Sea continental shelf. J. Geophys. Res. 101, 18519–18532 (1996).
Longhurst, A. R. & Harrison, W. G. The biological pump: profiles of plankton production and consumption in the upper ocean. Prog. Oceanogr. 22, 47–123 (1989).
Lewin, J. C. in Physiology and Biochemistry of Algae(ed. Lewin, R. E.) 445–455 (Academic, New York, (1962)).
Dugdale, R. C. & Wilkerson, F. P. Silicate regulation of new production in the equatorial Pacific upwelling. Nature 391, 270–273 (1998).
Nelson, D. M., Tréguer, P., Brzezinski, M. A., Leynaert, A. & Quéguiner, B. Production and dissolution of biogenic silica in the ocean: revised global estimates, comparison with regional data and relationship to biogenic sedimentation. Glob. Biogeochem. Cycles 9, 359–372 (1995).
Cole, J. J., Findlay, S. & Pace, M. L. Bacterioplankton production in fresh and saltwater ecosystems: a cross-system overview. Mar. Ecol. Prog. Ser. 43, 1–10 (1988).
Smith, D. C., Simon, M., Alldredge, A. L. & Azam, F. Intense hydrolytic enzyme activity on marine aggregates and implications for rapid particle dissolution. Nature 359, 139–142 (1992).
Smith, D. C., Steward, G. F., Long, R. A. & Azam, F. Bacterial utilization of carbon fluxes during a diatom bloom in a mesocosm. Deep-Sea Res. II 42, 75–97 (1995).
Kamatani, A. Dissolution rates of silica from diatoms decomposing at various temperatures. Mar. Biol. 68, 91–98 (1982).
Lewin, J. C. The dissolution of silica from diatom walls. Geochim. Geophys. Acta 21, 182–198 (1961).
Brzezinski, M. A. & Nelson, D. M. The annual silica cycle in the Sargasso Sea near Bermuda. Deep-Sea Res. I 42, 1215–1237 (1995).
Nelson, D. M. & Goering, J. J. Near-surface silica dissolution in the upwelling region off northwest Africa. Deep-Sea Res. 24, 65–73 (1977).
Brzezinski, M. A. & Nelson, D. M. Seasonal changes in the silicon cycle within a Gulf Stream warm-core ring. Deep-Sea Res. 36, 1009–1030 (1989).
Cowie, G. L. & Hedges, J. I. Digestion and alteration of the biochemical constituents of a diatom (Thalassiosira weissflogii) ingested by a herbivorous zooplankton (Calanus pacificus). Limnol. Oceanogr. 41, 581–594 (1996).
Tande, K. S. & Slagstad, D. Assimilation efficiency in herbivorous aquatic organisms — the potential of the ratio method using 14C and biogenic silica as markers. Limnol. Oceanogr. 30, 1093–1099 (1985).
Biddanda, B. A. & Pomeroy, L. R. Microbial aggregation and degradation of phytoplankton-derived detritus in seawater. I. Microbial succession. Mar. Ecol. Prog. Ser. 42, 79–88 (1988).
Brussaard, C. P. D.et al. Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar. Ecol. Prog. Ser. 123, 259–271 (1995).
Berges, J. A. & Falkowski, P. G. Physiological stress and cell death in marine phytoplankton: induction of proteases in response to nitrogen or light limitation. Limnol. Oceanogr. 43, 129–135 (1998).
Brussaard, C. P. D., Noordeloos, A. A. M. & Riegman, R. Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation. J. Phycol. 33, 980–987 (1997).
DeLong, E. Archael means and extremes. Science 280, 542–543 (1998).
Kröger, N., Bergsdorf, C. & Sumper, M. Anew calcium binding glycoprotein family constitutes a major diatom cell wall component. EMBO J. 13, 4676–4683 (1994).
Smayda, T. J. The suspension and sinking of phytoplankton in the sea. Oceanogr. Mar. Biol. Annu. Rev. 8, 353–414 (1970).
Kamatani, A. & Riley, J. P. Rate of dissolution of diatom silica walls in seawater. Mar. Biol. 55, 29–35 (1979).
Brzezinski, M. A., Alldredge, A. L. & O'Bryan, L. M. Silica cycling within marine snow. Limnol. Oceanogr. 42, 1706–1713 (1997).
Brzezinski, M. A., Phillips, D. R., Chavez, F. P., Friederich, G. E. & Dugdale, R. C. Silica production in the Monterey, California, upwelling system. Limnol. Oceanogr. 42, 1694–1705 (1997).
Parsons, T. R., Maita, Y. & Lalli, C. M. A Manual of Chemical and Biological Methods for Seawater Analysis(Pergamon, Oxford, (1984)).
Werner, D. Die Kieselsäure im Stoffwechsel von Cyclotella cryptica Reimann, Lewin und Guillard. Arch. Mikrobiol. 55, 278–308 (1966).
Hoppe, H. G. Significance of exoenzymatic activities in the ecology of brackish water: measurements by means of methylumbelliferyl-substrates. Mar. Ecol. Prog. Ser. 11, 299–308 (1983).
Smith, D. C. & Azam, F. Asimple, economical method for measuring bacterial protein synthesis rates in seawater using 3H-leucine. Mar. Microb. Food Webs 6, 107–114 (1992).
Lee, S. & Fuhrman, J. A. Relationships between biovolume and biomass of naturally derived marine bacterioplankton. Appl. Environ. Microbiol. 53, 1298–1303 (1987).
Acknowledgements
We thank D. C. Smith, M. Hildebrand, M. A. Brzezinski, J. T. Hollibaugh and K. A. Bidle for discussions and suggestions. This work was supported by NSF grants to F.A.
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Bidle, K., Azam, F. Accelerated dissolution of diatom silica by marine bacterial assemblages. Nature 397, 508–512 (1999). https://doi.org/10.1038/17351
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DOI: https://doi.org/10.1038/17351
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